Kim Lajoie

Cortical mechanisms involved in visuomotor coordination during precision walking

Goal-directed locomotion, in particular in situations where there is a need to step over or around obstacles, is largely guided by visual information. To negotiate an obstacle successfully, subjects must first plan how to perform the movement and then must execute that plan. In cats, this information must also be stored and used to guide the hindlimbs, which are moved in the absence of direct visual input. Experiments in cats have shown that the motor cortex makes an important contribution to the execution of gait modifications and is involved both in specifying limb trajectory and, when necessary, where the paw will be placed. We suggest that, in both situations, subpopulations of pyramidal tract neurons in the motor cortex act to regulate the duration, level and timing of small groups of synergistic muscles, active at different times during the gait modification. However, the available evidence suggests that the motor cortex plays little role in the planning of these gait modifications. Instead, recent work suggests that the posterior parietal cortex (PPC) may contribute to this function. In agreement with this proposal, we have found that lesions to this structure lead to errors in forelimb placement in front of an advancing obstacle and may produce deficits in forelimb-hindlimb coordination. Single-unit recordings from neurons in the PPC support a role for the PPC in these two aspects of visually guided locomotion and further show that the signal in this structure might be limb-independent.

Neurons in Area 5 of the Posterior Parietal Cortex in the Cat Contribute to Interlimb Coordination During Visually Guided Locomotion: A Role in Working Memory

We tested the hypothesis that area 5 of the posterior parietal cortex (PPC) contributes to interlimb coordination in locomotor tasks requiring visual guidance by recording neuronal activity in this area in three cats in two locomotor paradigms. In the first paradigm, cats were required to step over obstacles attached to a moving treadmill belt. We recorded 47 neurons that discharged in relationship to the hindlimbs. Of these, 31/47 discharged between the passage of the fore- and hindlimbs (FL-HL cells) over the obstacle. The activity of most of these neurons (25/31) was related to the fore- and hindlimb contralateral to the recording site when the contralateral forelimb was the first to pass over the obstacle. In many cells, discharge activity was limb-independent in that it was better related to the ipsilateral limbs when they were the first to step over the obstacle. The other 16/47 neurons discharged only when the hindlimbs stepped over the obstacle with the majority of these (12/16) discharging between the passage of the two hindlimbs over the obstacle. We tested 15/47 cells, including 11/47 FL-HL cells, in a second paradigm in which cats stepped over an obstacle on a walkway. Discharge activity in all of these cells was significantly modulated when the cat stepped over the obstacle and remained modified for periods of ≤ 1 min when forward progress of the cat was delayed with either the fore- and hindlimbs, or the two hindlimbs, straddling the obstacle. We suggest that neurons in area 5 of the PPC contribute to interlimb coordination during locomotion by estimating the spatial and temporal attributes of the obstacle with respect to the body. We further suggest that the discharge observed both during the steps over the obstacle and in the delayed locomotor paradigm is a neuronal correlate of working memory.

A Contribution of Area 5 of the Posterior Parietal Cortex to the Planning of Visually Guided Locomotion: Limb-Specific and Limb-Independent Effects

We tested the hypothesis that area 5 of the posterior parietal cortex (PPC) contributes to the planning of visually guided gait modifications. We recorded 121 neurons from the PPC of two cats during a task in which cats needed to process visual input to step over obstacles attached to a moving treadmill belt. During unobstructed locomotion, 64/121 (53%) of cells showed rhythmic activity. During steps over the obstacles, 102/121 (84%) of cells showed a significant change of their activity. Of these, 46/102 were unmodulated during the control task. We divided the 102 task-related cells into two groups on the basis of their discharge when the limb contralateral to the recording site was the first to pass over the obstacle. One group (41/102) was characterized by a brief, phasic discharge as the lead forelimb passed over the obstacle (Step-related cells). These cells were recorded primarily from area 5a. The other group (61/102) showed a progressive increase in activity prior to the onset of the swing phase in the modified limb and frequently diverged from control at least one step cycle before the gait modification (Step-advanced cells). Most of these cells were recorded in area 5b. In both groups, some cells maintained a fixed relationship to the activity of the contralateral forelimb regardless of which limb was the first to pass over the obstacle (limb-specific cells), whereas others changed their phase of activity so that they were always related to activity of the first limb to pass over the obstacle, either contralateral or ipsilateral (limb-independent cells). Limb-independent cells were more common among the Step-advanced cell population. We suggest that both populations of cells contribute to the gait modification and that the discharge characteristics of the Step-advanced cells are compatible with a contribution to the planning of the gait modification.

The contribution of vision, proprioception, and efference copy in storing a neural representation for guiding trail leg trajectory over an obstacle

Stepping over obstacles requires vision to guide the leading leg, but direct visual information is not available to guide the trailing leg. The neural mechanisms for establishing a stored obstacle representation and thus facilitating the trail leg trajectory in humans are unknown. Twenty-four subjects participated in one of three experiments, which were designed to investigate the contribution of visual, proprioceptive, and efference copy signals. Subjects stepped over an obstacle with their lead leg, stopped, and straddled the obstacle for a delay period before stepping over it with their trail leg while toe elevation was recorded. Subsequently, we calculated maximum toe elevation and toe clearance. First, we found that subjects could accurately scale trail leg toe elevation and clearance, despite straddling an obstacle for up to 2 min, similar to quadrupeds. Second, we found that when the lead leg was passively moved over an obstacle (eliminating an efference copy signal and altering proprioception) without vision, trail leg toe elevation and clearance were reduced, and variability increased compared with when subjects actively moved their lead leg. Trail leg toe measures returned to normal when vision was provided during the passive manipulation. Finally, we found that altering lead leg proprioceptive feedback by adding mass to the ankle had no effect on trail leg toe measures. Taken together, our results suggest that humans can store a neural representation of obstacle properties for extended periods of time and that vision appears to be sufficient in this process to guide trail leg trajectory.

Chapter 6 - Motor planning of locomotor adaptations on the basis of vision: The role of the posterior parietal cortex

In this chapter, we consider the contribution of the posterior parietal cortex (PPC) to obstacle avoidance behavior and we define a model that identifies the major planning processes that are required for this task. A key aspect of this planning process is the need to integrate information concerning the obstacle, obtained from vision, together with an estimation of body and limb state. We suggest that the PPC makes a major contribution to this process during visually guided locomotion. We present evidence from lesion and single unit recording experiments in the cat that are compatible with this viewpoint.

Effect of ambient light and age-related macular degeneration on precision walking.

Purpose To determine how age-related macular degeneration (AMD) and changes in ambient light affect the control of foot placement while walking. Methods Ten older adults with AMD and 11 normal-sighted controls performed a precision walking task under normal (∼600 lx), dim (∼0.7 lx), and after a sudden reduction (∼600 to 0.7 lx) of light. The precision walking task involved subjects walking and stepping to the center of a series of irregularly spaced, low-contrast targets. Habitual visual acuity and contrast sensitivity and visual field function were also assessed. Results There were no differences between groups when performing the walking task in normal light (p > 0.05). In reduced lighting, older adults with AMD were less accurate and more variable when stepping across the targets compared to controls (p < 0.05). A sudden reduction of light proved the most challenging for this population. In the AMD group, contrast sensitivity and visual acuity were not significantly correlated with walking performance. Visual field thresholds in the AMD group were only associated with greater foot placement error and variability in the dim light walking condition (r = −0.69 to −0.87, p < 0.05). Conclusions While walking performance is similar between groups in normal light, poor ambient lighting results in decreased foot placement accuracy in older adults with AMD. Improper foot placement while walking can lead to a fall and possible injury. Thus, to improve the mobility of those with AMD, strategies to enhance the environment in reduced lighting situations are necessary.

Effects of age-related macular degeneration and ambient light on curb negotiation

Purpose To determine how age-related macular degeneration (AMD) and changes in ambient light affect the ability to negotiate a curb while walking. Methods Ten older adults with AMD and 11 normal-sighted control subjects performed a curb negotiation task under normal light (∼600 lux), dim light (∼0.7 lux), and following a sudden reduction (∼600 to 0.7 lux) of light. In this task, subjects walked and stepped up or down a simulated sidewalk curb. Movement kinematics and ground reaction forces were measured during curb ascent and descent. Habitual visual acuity, contrast sensitivity, and visual fields were also assessed. Results Apart from slower gait speed in those with AMD, there were no differences between groups during curb ascent for any other measure. During curb descent, older adults with AMD frequently used shuffling steps in the approach phase to locate the curb edge and showed prolonged double support duration stepping over the curb compared with control subjects. However, reduced lighting, particularly a sudden reduction, led to several significant changes in movement characteristics in both groups. For instance, toe clearance stepping up the curb was greater, and landing force stepping down was reduced. In addition, slower gait speed and greater double support duration were evident in curb ascent and descent. In AMD subjects, contrast sensitivity, visual acuity, and visual field threshold were associated with several kinematic measures in the three light conditions during curb negotiation. Conclusions Minor AMD-specific changes in movement are seen during curb negotiation. However, attenuated lighting greatly impacts curb ascent and descent, regardless of eye disease, which manifests as a cautious walking strategy and may increase the risk of falling. Environmental enhancements that reduce the deleterious effects of poor lighting are required to improve mobility and quality of life of older adults, particularly those with AMD.

Modification of cutaneous reflexes during visually guided walking.

Although it has become apparent that cutaneous reflexes can be adjusted based on the phase and context of the locomotor task, it is not clear to what extent these reflexes are regulated when locomotion is modified under visual guidance. To address this, we compared the amplitude of cutaneous reflexes while subjects performed walking tasks that required precise foot placement. In one experiment, subjects walked overground and across a horizontal ladder with narrow raised rungs. In another experiment, subjects walked and stepped onto a series of flat targets, which required different levels of precision (large vs. narrow targets). The superficial peroneal or tibial nerve was electrically stimulated in multiple phases of the gait cycle in each condition and experiment. Reflexes between 50 and 120 ms poststimulation were sorted into 10 equal phase bins, and the amplitudes were then averaged. In each experiment, differences in cutaneous reflexes between conditions occurred predominantly during swing phase when preparation for precise foot placement was necessary. For instance, large excitatory cutaneous reflexes in ipsilateral tibialis anterior were present in the ladder condition and when stepping on narrow targets compared with inhibitory responses in the other conditions, regardless of the nerve stimulated. In the ladder experiments, additional effects of walking condition were evident during stance phase when subjects had to balance on the narrow ladder rungs and may be related to threat and/or the unstable foot-surface interaction. Taken together, these results suggest that cutaneous reflexes are modified when visual feedback regarding the terrain is critical for successful walking.

Coordination of Gaze Behavior and Foot Placement During Walking in Persons with Glaucoma

Purpose: Vision normally provides environmental information necessary to direct the foot to safe locations during walking. Peripheral visual field loss limits what a person can see, and may alter how a person visually samples the environment. Here we tested the hypothesis that the spatial-temporal coupling between gaze and stepping in a precision-based walking task is altered in persons with glaucoma, particularly under dual task situations, and results in reduced foot-placement accuracy. Methods: Twenty persons with glaucoma and 20 normally sighted controls performed a precision walking task that involved stepping to the center of 4 targets under 3 conditions: targets only, walking, and counting backwards to simulate a conversation, and walking while performing a concurrent visual search task to simulate locating a landmark. We quantified foot-placement error and error variability with respect to the targets, as well as saccade and fixation timing with respect to foot placement. Results: Compared with controls, persons with glaucoma looked earlier at future stepping targets (with respect to toe-off of the foot) in the targets only and count conditions, and transferred gaze away sooner from the current stepping target in all conditions (P<0.05). Persons with glaucoma also had increased foot-placement error, particularly in the count condition, and increased foot-placement error variability compared with normally sighted controls (P<0.05). Conclusions: Glaucoma significantly disrupts gaze-foot coordination and results in less accurate foot placement when precision is required during walking. This may increase the risk of trips and falls in this population.

Glaucoma-Related Differences in Gaze Behavior When Negotiating Obstacles

Purpose Safe navigation requires avoiding objects. Visual field loss may affect how one visually samples the environment, and may thus contribute to bumping into objects and falls. We tested the hypothesis that gaze strategies and the number of collisions differ between people with glaucoma and normally sighted controls when navigating around obstacles, particularly under multitasking situations. Methods Twenty persons with moderate–severe glaucoma and 20 normally sighted controls walked around a series of irregularly spaced vertical obstacles under the following three conditions: walking with obstacles only, walking and counting backward to simulate a conversation, and walking while performing a concurrent visual search task to simulate locating a landmark. We quantified gaze patterns and the number of obstacle contacts. Results Compared with controls, people with glaucoma directed gaze closer to their current position (P < 0.05). They also directed a larger proportion of fixations (in terms of number and duration) to obstacles (P < 0.05). Despite this finding, considerably more people with glaucoma contacted an obstacle (P < 0.05). Multitasking led to changes in gaze behavior in both groups, and this was accompanied by a large increase in obstacle contacts among those with glaucoma (P < 0.05). Conclusions Glaucoma alters gaze patterns when negotiating a series of obstacles and increases the likelihood of collisions. Multitasking in this situation exacerbates these changes. Translational Relevance Understanding glaucoma-related changes in gaze behavior during walking in cluttered environments may provide critical insight for orientation and mobility specialists and guide the design of gaze training interventions to improve mobility.